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Harperocallis Is Congeneric with Isidrogalvia (Tofieldiaceae, Alismatales): Evidence from Comparative Floral Morphology

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Harperocallis Is Congeneric with Isidrogalvia (Tofieldiaceae, Alismatales): Evidence from Comparative Floral Morphology TAXON 19 July 2011: 19 pp. Remizowa & al. • Classification of Tofieldiaceae MORPHOLOGY Harperocallis is congeneric with Isidrogalvia (Tofieldiaceae, Alismatales): Evidence from comparative floral morphology Margarita V. Remizowa,1 Dmitry D. Sokoloff,1 Lisa M. Campbell,2 Dennis W. Stevenson2 & Paula J. Rudall3 1 Department of Higher Plants, Faculty of Biology, Moscow State University, Moscow, 119991, Russia 2 New York Botanical Garden, Bronx, New York 10458, U.S.A. 3 Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, U.K. Author for correspondence: Margarita Remizowa, [email protected] Abstract Flowers of most Tofieldiaceae are inserted laterally in the axils of well-developed flower-subtending bracts in a racemose inflorescence, each flower possessing a characteristic calyculus. The monospecific genus Harperocallis, which is endemic to north-western Florida, represents the only member of Tofieldiaceae with a consistently solitary terminal flower. We compare flowers of H. flava with those of Isidrogalvia, a putative close relative of Harperocallis from South America. We analyse the resulting data in an extended morphological analysis for the entire family. Both Harperocallis and Isidrogalvia lack septal nectaries, which are functionally replaced by tuberculate glands on the ovary walls; in both genera the carpels are united with congenital carpel fusion at the gynoecium base. Flowers of both genera are relatively large and highly vas- cularized; the calycular phyllomes and tepals each possess several veins and the carpels contain (in addition to dorsal and ventral bundles) both lateral bundles and separate placental bundles that support massive intrusive placentae. The presence of a synascidiate zone with congenital intercarpellary fusion in both genera is correlated with the formation of heterocar- pellary ventral bundles. Harperocallis is unusual in that the stamens are often supplied by three veins. Our morphological cladistic analysis supports earlier molecular data indicating a close relationship between Harperocallis and Isidrogalvia, and several morphological characters are revealed as synapomorphies of this sister-pairing. This finding, resulting from strong morphological similarities between Harperocallis and Isidrogalvia, allows the transfer of H. flava into Isidrogalvia. Keywords floral anatomy; gynoecium; Harperocallis; Isidrogalvia; Tofieldiaceae INTRODUCTION three genera that contain more than one species (Isidrogal- via, Tofieldia, Triantha) was found to be monophyletic. Pleea The monocot family Tofieldiaceae includes five genera was strongly supported as a sister to all other Tofieldiaceae, (Harperocallis McDaniel, Isidrogalvia Ruiz & Pav., Pleea which fall into two distinct clades: (1) Tofieldia + Triantha and Michx., Tofieldia Huds., Triantha (Nutt.) Baker) distributed (2) Isidrogalvia + Harperocallis; thus their phylogenetic re- in Eurasia, North America, and South America. Based on re- construction is summarized as Pleea ((Tofieldia + Triantha) + cent molecular phylogenies, Tofieldiaceae are placed in the (Isidrogalvia + Harperocallis)). Based on their results, Azuma order Alismatales (APG, 1998; Qiu & al., 2000; Chase & al., & Tobe (2010) hypothesized that the possession of six (rather 2000, 2006; Chase, 2004; Davis & al., 2004; Givnish & al., than nine) stamens per flower represents a synapomorphy of 2006; Graham & al., 2006; APG III, 2009). Tofieldiaceae are all Tofieldiaceae except Pleea, a problematic conclusion that well defined by several synapomorphies, of which the most requires further discussion in a broader context of androe- important is a structure termed a calyculus, which represents cium evolution in all lineages of early-divergent monocots three involucral phyllomes surrounding the flower (Takhta- (Endress, 1995; Ronse De Craene & Smets, 1995; Remizowa jan, 1994, 1997, 2009; Zomlefer, 1997; Remizowa & Sokoloff & al., 2010b). Azuma & Tobe (2010) further hypothesized that 2003; Remizowa & al., 2006a, 2010a; Azuma & Tobe 2010). an inflorescence axis bearing glandular trichomes is a syn- In all genera of Tofieldiaceae except Harperocallis, flowers apomorphy of Triantha, and that free calycular phyllomes are are lateral and situated in the axils of well-developed flower- a synapomorphy of Harperocallis + Isidrogalvia. They con- subtending bracts (Takhtajan, 1994, 1997, 2009; Zomlefer, cluded that most intergeneric relationships in Tofieldiaceae 1997; Remizowa & Sokoloff 2003; Remizowa & al., 2006a, have weak or no support from morphological characters and 2010a), though a terminal flower is also occasionally present recommended a comparative morphological study of the genera (Remizowa, 2007). Harperocallis differs considerably from all (Azuma & Tobe, 2010). the other genera in consistently possessing a single terminal Extensive comparative studies on the floral morphology flower. and anatomy of Tofieldiaceae (summarized below) have in- Azuma & Tobe (2010) conducted a molecular phylogenetic dicated that floral data are useful as phylogenetic markers in study including all genera of Tofieldiaceae. They found that the group. However, many gaps remain, especially with re- the monophyly of Tofieldiaceae is well supported. Each of the spect to the monospecific Harperocallis, which is the most 1 Remizowa & al. • Classification of Tofieldiaceae TAXON 19 July 2011: 19 pp. enigmatic genus of the family (Zomlefer, 1997). Harperocallis base (Zomlefer, 1997). The ovary with tuberculate emergences flava McDaniel is narrowly endemic to the western Florida is also highlighted as a unique feature (autapomorphy) of Har- Panhandle, where it has a relatively limited range and very low perocallis (Ambrose, 1980; Cruden, 1991; Zomlefer, 1997). The infraspecific genetic diversity (Godt & al., 1997). Surprisingly, floral anatomy of Harperocallis was studied by Utech (1993), this remarkable species with relatively large and showy flow- who reported a multi-bundled pedicel and a simple axial vas- ers was described relatively recently (McDaniel, 1968). In this cular system of a single terminal flower. According to Utech study, we re-examine the floral anatomy of Isidrogalvia and (1993), the carpels are nearly apocarpous and supplied by three Harperocallis with particular respect to gynoecium structure. veins each, one dorsal and two ventrals. Both of these genera are relatively poorly known in contrast Using a morphological cladistic analysis, we explore with Tofieldia and its allies. whether data on floral morphology are congruent with the Tofieldia and Triantha are characterized by small flowers molecular-based conclusion that Harperocallis and Isidro- each surrounded by united calyculus phyllomes. Calyculus galvia form a sister pair (Azuma & Tobe, 2010). Earlier mor- phyllomes, tepals (in most species), and stamens are each sup- phology-based studies have revealed contrasting relationships plied by a single vein (Anderson, 1940; El-Hamidi, 1952; Eie, among the taxa currently assigned to Tofieldiaceae. Ambrose 1972; Utech, 1978; Sterling, 1979; Remizowa & al., 2010a). The (1980) conducted a numerical (phenetic) analysis of “Lilia- gynoecium is syncarpous and consists of three postgenitally ceae-Melanthioideae”, a polyphyletic group that includes taxa united stipitate carpels. The ovary is trilocular (usually a short currently placed in quite different families and orders: Tofiel- unilocular region is also present in the middle part of the ovary) diaceae (Alismatales), Nartheciaceae (Dioscoreales), Colchi- and possesses infralocular septal (gynopleural) nectaries. Each caceae and Melanthiaceae (Liliales). In analyses of a matrix carpel consists of a short sterile ascidiate zone and a long fertile containing 19 species and 110 characters, a dendrogram for the plicate zone. The carpel stipes, stylodia, and stigmas are free genera of Tofieldiaceae (Ambrose, 1980) was topologically the (Takhtajan, 1994, 1997; Zomlefer, 1997; Smets & al., 2000; Ig- same as the phylogenetic tree of Azuma & Tobe (2010). When ersheim & al., 2001; Rudall, 2002; Remizowa & Sokoloff, 2003; 28 species and 71 characters were analysed (Ambrose, 1980), Remizowa & al., 2006b, 2010a). Each carpel is individually the following clustering was found: Pleea (Triantha (Tofieldia vascularized with a dorsal and a ventral vein. The ventral vein (Harperocallis + Isidrogalvia))). Cruden (1991) conducted a cla- divides into two strands in the cross-zone (Anderson, 1940; distic analysis based on 36 morphological characters scored for Utech, 1978; Sterling, 1979; Remizowa & al., 2010a). ten species of Tofieldiaceae (including members of all genera) Isidrogalvia differs from Tofieldia + Triantha (and Pleea) plus an outgroup based on characters of Aletris, Narthecium by possession of free calyculus phyllomes, large flowers, te- and Nietneria, which are now placed in Nartheciaceae, in a pals supplied by numerous veins and other characters (Сruden, different order, Dioscoreales (APG III, 2009). When all 36 1991; Zomlefer, 1997). With about ten species (Cruden, 1991; characters were considered, Isidrogalvia was monophyletic; Campbell, 2010), Isidrogalvia is one of the two largest gen- Isidrogalvia and Harperocallis formed two successive basal era of the family (together with Tofieldia) and represents the branches on a cladogram. When some morphological data only South American member. Sterling (1979) examined the were omitted, Isidrogalvia was either paraphyletic or sister to gynoecium anatomy of some species of Isidrogalvia (along Pleea.
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